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Applied Microbiology and Biotechnology

, Volume 102, Issue 12, pp 5235–5244 | Cite as

Inorganic polyphosphate in methylotrophic yeasts

  • Nadeshda Andreeva
  • Lubov Ryazanova
  • Anton Zvonarev
  • Ludmila Trilisenko
  • Tatiana Kulakovskaya
  • Mikhail Eldarov
Applied microbial and cell physiology

Abstract

Inorganic polyphosphate (polyP) is a significant regulatory and metabolic compound in yeast cells. We compared polyP content and localization, polyphosphatase activities, and transcriptional profile of polyP-related genes in industrially important methylotrophic yeasts, Hansenula polymorpha and Pichia pastoris. The increased need for phosphate, the decrease of long-chain polyP level, the accumulation of short-chain polyP, and enhanced endopolyphosphatase activity in the crude membrane fraction were observed in methanol-grown cells compared with glucose-grown cells of both species. Transcriptome analysis revealed notable differences in the expression patterns of key genes encoding proteins related to polyP metabolism. In methanol-grown cells, the genes encoding endopolyphosphatases and phosphate transporters were upregulated. The changes in polyP metabolism are probably related to the peculiarities of bioenergetics of methanol-grown cells.

Keywords

Polyphosphate Polyphosphatase Methylotrophic yeast Hansenula polymorpha Pichia pastoris Transcriptome 

Notes

Acknowledgements

The authors thank Elena Makeeva for her help with preparing the manuscript.

Funding

This study was funded by the Russian Foundation for Basic Research (Grant No. 17-04-00822).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2018_9008_MOESM1_ESM.pdf (2.4 mb)
ESM 1 (PDF 2465 kb)

References

  1. Achbergerová L, Nahálka J (2011) Polyphosphate-an ancient energy source and active metabolic regulator. Microb Cell Factories 10:63.  https://doi.org/10.1186/1475-2859-10-63 CrossRefGoogle Scholar
  2. Albi T, Serrano A (2016) Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J Microbiol Biotechnol 32(2):27.  https://doi.org/10.1007/s11274-015-1983-2 CrossRefPubMedGoogle Scholar
  3. Andreeva NA, Okorokov LA (1993) Purification and characterization of highly active and stable polyphosphatase from Saccharomyces cerevisiae cell envelope. Yeast 9:127–139CrossRefPubMedGoogle Scholar
  4. Andreeva N, Trilisenko L, Eldarov M, Kulakovskaya T (2015) Polyphosphatase PPN1 of Saccharomyces cerevisiae: switching of exopolyphosphatase and endopolyphosphatase activities. PLoS One 10(3):e0119594.  https://doi.org/10.1371/journal.pone.0119594 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aschar-Sobbi R, Abramov AY, Diao C, Kargacin ME, Kargacin GJ, French RJ, Pavlov E (2008) High sensitivity, quantitative measurements of polyphosphate using a new DAPI-based approach. J Fluoresc 18(5):859–866.  https://doi.org/10.1007/s10895-008-0315-4 CrossRefPubMedGoogle Scholar
  6. Bensadoun A, Weinstein D (1976) Assay of proteins in the presence of interfering materials. Anal Biochem 70:241–250CrossRefPubMedGoogle Scholar
  7. Byrne B (2015) Pichia pastoris as an expression host for membrane protein structural biology. Curr Opin Struct Biol 32:9–17.  https://doi.org/10.1016/j.sbi.2015.01.005 CrossRefPubMedGoogle Scholar
  8. Chávez FP, Lünsdorf H, Jerez CA (2004) Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chlorobiphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. Appl Environ Microbiol 70:3064–3072CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clotet J (2017) Polyphosphate: popping up from oblivion. Curr Genet 63:15–18CrossRefPubMedGoogle Scholar
  10. Collart MA, Oliviero S (2001) Preparation of yeast RNA. Curr Protoc Mol Biol Chapter 13:Unit13.12.  https://doi.org/10.1002/0471142727.mb1312s23
  11. Costa C, Giménez-Capitán A, Karachaliou N, Rosell R (2013) Comprehensive molecular screening: from the RT-PCR to the RNA-seq. Transl Lung Cancer Res 2:87–91.  https://doi.org/10.3978/j.issn.2218-6751.2013.02.05 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Culotta VC, Daly MJ (2013) Manganese complexes: diverse metabolic routes to oxidative stress resistance in prokaryotes and yeast. Antioxid Redox Signal 19(9):933–944.  https://doi.org/10.1089/ars.2012.5093 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gasser B, Prielhofer R, Marx H, Maurer M, Nocon J, Steiger M, Puxbaum V, Sauer M, Mattanovich D (2013) Pichia pastoris: protein production host and model organism for biomedical research. Future Microbiol 8:191–208.  https://doi.org/10.2217/fmb.12.133 CrossRefPubMedGoogle Scholar
  14. Gasser B, Steiger MG, Mattanovich D (2015) Methanol regulated yeast promoters: production vehicles and toolbox for synthetic biology. Microb Cell Factories 14:196.  https://doi.org/10.1186/s12934-015-0387-1 CrossRefGoogle Scholar
  15. Gerasimait R, Mayer A (2017) Ppn2, a novel Zn2+-dependent polyphosphatase in the acidocalcisome-like yeast vacuole. J Cell Sci 130:1625–1636.  https://doi.org/10.1242/jcs.201061 CrossRefGoogle Scholar
  16. Gray MJ, Jakob U (2015) Oxidative stress protection by polyphosphate—new roles for an old player. Curr Opin Microbiol 24:1–6.  https://doi.org/10.1016/j.mib.2014.12.004 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, Uttenweiler A, Reinhardt M, Schmidt A, Seiler J, Ladurner AG, Herrmann C, Scheffzek K, Mayer A (2009) Catalytic core of a membrane-associated eucaryotic polyphosphate polymerase. Science 324:513–516CrossRefPubMedGoogle Scholar
  18. Kulaev IS, Vagabov VM, Kulakovskaya TV (2004) The biochemistry of inorganic polyphosphates. John Wiley & Sons Ltd, ChichesterCrossRefGoogle Scholar
  19. Kulakovskaya TV, Andreeva NA, Karpov A, Sidorov I, Kulaev IS (1999) Hydrolysis of tripolyphosphate by purified exopolyphosphatase of Saccharomyces cerevisiae cytosol: kinetic model. Biochem Mosc 64:990–993Google Scholar
  20. Kumble KD, Kornberg A (1995) Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem 270:5818–5822CrossRefPubMedGoogle Scholar
  21. Kunze G, Kang HA, Gellissen G (2009) Hansenula polymorpha (Pichia angusta): biology and applications. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer Netherlands, Dordrecht, pp 47–64.  https://doi.org/10.1007/978-1-4020-8292-4_3 CrossRefGoogle Scholar
  22. Kuroda A (2006) A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci Biotechnol Biochem 70(2):325–331CrossRefPubMedGoogle Scholar
  23. Kurtzman CP (2009) Biotechnological strains of Komagataella (Pichia) pastoris are Komagataella phaffii as determined from multigene sequence analysis. J Ind Microbiol Biotechnol 36:1435–1438.  https://doi.org/10.1007/s10295-009-0638-4 CrossRefPubMedGoogle Scholar
  24. Liang S, Wang B, Pan L, Ye Y, He M, Han S, Zheng S, Wang X, Lin Y (2012) Comprehensive structural annotation of Pichia pastoris transcriptome and the response to various carbon sources using deep paired-end RNA sequencing. BMC Genomics 13:738.  https://doi.org/10.1186/1471-2164-13-738 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lichko L, Kulakovskaya T, Pestov N, Kulaev I (2006) Inorganic polyphosphates and exopolyphosphatases in cell compartments of the yeast Saccharomyces cerevisiae under inactivation of PPX1 and PPN1 genes. Biosci Rep 26:45–54CrossRefPubMedGoogle Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  27. Lonetti A, Szijgyarto Z, Bosch D, Loss O, Azevedo C, Saiardi A (2011) Identification of an evolutionarily conserved family of inorganic polyphosphate endopolyphosphatases. J Biol Chem 286:31966–31974CrossRefPubMedPubMedCentralGoogle Scholar
  28. Love KR, Shah KA, Whittaker CA, Wu J, Bartlett MC, Ma D, Leeson RL, Priest M, Borowsky J, Young SK, Love JC (2016) Comparative genomics and transcriptomics of Pichia pastoris. BMC Genomics 17:550.  https://doi.org/10.1186/s12864-016-2876-y CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mattanovich D, Sauer M, Gasser B (2016) Industrial microorganisms: Pichia pastoris. In: Industrial biotechnology. In: Wittmann C, Liao JC (eds) Verlag GmbH & Co. KGaA, Weinheim, Germany, p 687–714. doi:  https://doi.org/10.1002/9783527807796.ch19Wiley-VCH
  30. Müller WEG, Wang S, Neufurth M, Kokkinopoulou M, Feng Q, Schröder HC, Wang X (2017) Polyphosphate as donor of high-energy phosphate for the synthesis of ADP and ATP. J Cell Sci 130(16):2747–2756.  https://doi.org/10.1242/jcs.204941 CrossRefPubMedGoogle Scholar
  31. Nikel PI, Chavarría M, Martínez-García E, Taylor AC, de Lorenzo V (2013) Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440. Microb Cell Factories 12:50.  https://doi.org/10.1186/1475-2859-12-50 CrossRefGoogle Scholar
  32. Numamoto M, Maekawa H, Kaneko Y (2017) Efficient genome editing by CRISPR/Cas9 with a tRNA-sgRNA fusion in the methylotrophic yeast Ogataea polymorpha. J Biosci Bioeng 124(5):487–492.  https://doi.org/10.1016/j.jbiosc.2017.06.001 CrossRefPubMedGoogle Scholar
  33. Omelon S, Georgiou J, Habraken W (2016) A cautionary (spectral) tail: red-shifted fluorescence by DAPI-DAPI interactions. Biochem Soc Trans 2016 Feb 44(1):46–49.  https://doi.org/10.1042/BST20150231 CrossRefPubMedGoogle Scholar
  34. Puntus IF, Ryazanova LP, Zvonarev AN, Funtikova TV, Kulakovskaya TV (2015) The role of mineral phosphorus compounds in naphthalene biodegradation by Pseudomonas putida. Appl Biochem Microbiol 51:202–208CrossRefGoogle Scholar
  35. Rao NN, Gómez-García MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78:605–647CrossRefPubMedGoogle Scholar
  36. Ravin NV, Eldarov MA, Kadnikov VV, Beletsky AV, Schneider J, Mardanova ES, Smekalova EM, Zvereva MI, Dontsova OA, Mardanov AV, Skryabin KG (2013) Genome sequence and analysis of methylotrophic yeast Hansenula polymorpha DL1. BMC Genomics 14:837.  https://doi.org/10.1186/1471-2164-14-837 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Riley R, Haridas S, Wolfe KH, Lopes MR, Hittinger CT, Göker M, Salamov AA, Wisecaver JH, Long TM, Calvey CH, Aerts AL, Barry KW, Choi C, Clum A, Coughlan AY, Deshpande S, Douglass AP, Hanson SJ, Klenk HP, LaButti KM, Lapidus A, Lindquist EA, Lipzen AM, Meier-Kolthoff JP, Ohm RA, Otillar RP, Pangilinan JL, Peng Y, Rokas A, Rosa CA, Scheuner C, Sibirny AA, Slot JC, Stielow JB, Sun H, Kurtzman CP, Blackwell M, Grigoriev IV, Jeffries TW (2016) Comparative genomics of biotechnologically important yeasts. Proc Natl Acad Sci U S A 113:9882–9887, doi: https://doi.org/10.1073/pnas.1603941113
  38. Roohvand F, Shokri M, Abdollahpour-Alitappeh M, Ehsani P (2017) Biomedical applications of yeast—a patent view, part one: yeasts as workhorses for the production of therapeutics and vaccines. Expert Opin Ther Pat 27(8):929–951.  https://doi.org/10.1080/13543776.2017.1339789 CrossRefPubMedGoogle Scholar
  39. Rubin GM (1973) The nucleotide sequence of Saccharomyces cerevisiae 5.8S ribosomal ribonucleic acid. J Biol Chem 11:3860–3875Google Scholar
  40. Rußmayer H, Buchetics M, Gruber C, Valli M, Grillitsch K, Modarres G, Guerrasio R, Klavins K, Neubauer S, Drexler H, Steiger M, Troyer C, Chalabi A, Krebiehl G, Sonntag D, Zellnig G, Daum G, Graf AB, Altmann F, Koellensperger G, Hann S, Sauer M, Mattanovich D, Gasser B (2015) Systems-level organization of yeast methylotrophic lifestyle. BMC Biol 13:80.  https://doi.org/10.1186/s12915-015-0186-5 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Serafim LS, Lemos OC, Levantesi C, Tandoi V, Santos H, Reis MA (2002) Methods for detection and visualization of intracellular polymers stored by polyphosphate-accumulating microorganisms. J Microbiol Meth 51:1–18CrossRefGoogle Scholar
  42. Shabalin YA, Vagabov VM, Tsiomenko AB, Zemlianuhina OA, Kulaev IS (1977) Study of polyphosphate kinase activity in the yeast vacuoles. Biokhimia (Moscow) 42:1642–1648Google Scholar
  43. Spohner SC, Müller H, Quitmann H, Czermak P (2015) Expression of enzymes for the usage in food and feed industry with Pichia pastoris. J Biotechnol 202:118–134.  https://doi.org/10.1016/j.jbiotec.2015.01.027 CrossRefPubMedGoogle Scholar
  44. Sturmberger L, Chappell T, Geier M, Krainer F, Day KJ, Vide U, Trstenjak S, Schiefer A, Richardson T, Soriaga L, Darnhofer B, Birner-Gruenberger R, Glick BS, Tolstorukov I, Cregg J, Madden K, Glieder A (2016) Refined Pichia pastoris reference genome sequence. J Biotechnol 235:121–231.  https://doi.org/10.1016/j.jbiotec.2016.04.023 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tomàs-Gamisans M, Ferrer P, Albiol J (2016) Integration and validation of the genome-scale metabolic models of Pichia pastoris: a comprehensive update of protein glycosylation pathways, lipid and energy metabolism. PLoS One 11:e0148031.  https://doi.org/10.1371/journal.pone.0148031 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Trilisenko LV, Andreeva NA, Eldarov MA, Dumina MV, Kulakovskaya TV (2015) Polyphosphates and polyphosphatase activity in the yeast Saccharomyces cerevisiae during overexpression of the DDP1 gene. Biochemistry (Mosc) 80:1312–1317.  https://doi.org/10.1134/S0006297915100120 CrossRefGoogle Scholar
  47. Vagabov VM, Trilisenko LV, Kulakovskaya TV, Kulaev IS (2008) Еffect of carbon source on polyphosphate accumulation in Saccharomyces cerevisiae. FEMS Yeast Res 8:877–882CrossRefPubMedGoogle Scholar
  48. Valli M, Tatto NE, Peymann A, Gruber C, Landes N, Ekker H, Thallinger GG, Mattanovich D, Gasser B, Graf AB (2016) Curation of the genome annotation of Pichia pastoris (Komagataella phaffii) CBS7435 from gene level to protein function. FEMS Yeast Res 16(6):fow051.  https://doi.org/10.1093/femsyr/fow051 CrossRefPubMedGoogle Scholar
  49. van Dijken JP, Otto R, Harder W (1975) Oxidation of methanol, formaldehyde and formate by catalase purified from methanol-grown Hansenula polymorpha. Arch Microbiol 31;106(3):221–226CrossRefGoogle Scholar
  50. van Zutphen T, Baerends RJS, Susanna KA, de Jong A, Kuipers OP, Veenhuis M, van der Klei IJ (2010) Adaptation of Hansenula polymorpha to methanol: a transcriptome analysis. BMC Genomics 11(1):1.  https://doi.org/10.1186/1471-2164-11-1 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Vogl T, Glieder A (2013) Regulation of Pichia pastoris promoters and its consequences for protein production. New Biotechnol 30:385–404.  https://doi.org/10.1016/j.nbt.2012.11.010 CrossRefGoogle Scholar
  52. Wagner JM, Alper HS (2016) Synthetic biology and molecular genetics in non-conventional yeasts: current tools and future advances. Fungal Genet Biol 89:126–136.  https://doi.org/10.1016/j.fgb.2015.12.001 CrossRefPubMedGoogle Scholar
  53. Weninger A, Hatzl A-M, Schmid C, Vogl T, Glieder A (2016) Combinatorial optimization of CRISPR/Cas9 expression enables precision genome engineering in the methylotrophic yeast Pichia pastoris. J Biotechnol 235:139–149.  https://doi.org/10.1016/j.jbiotec.2016.03.027 CrossRefPubMedGoogle Scholar
  54. Wurst H, Shiba T, Kornberg A (1995) The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J Bacteriol 177:898–906CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yamada Y, Maeda K, Mikata K (1994) The phylogenetic relationships of the hat-shaped ascospore-forming, nitrate-assimilating Pichia species, formerly classified in the genus Hansenula Sydow et Sydow, based on the partial sequences of 18S and 26S ribosomal RNAs (Saccharomycetaceae): the proposals of three new genera, Ogataea, Kuraishia, and Nakazawaea. Biosci Biotechnol Biochem 58:1245–1257CrossRefPubMedGoogle Scholar
  56. Yurimoto H, Oku M, Sakai Y (2011) Yeast methylotrophy: metabolism, gene regulation and peroxisome homeostasis. Int J Microbiol 2011:101298–101298.  https://doi.org/10.1155/2011/101298 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Nadeshda Andreeva
    • 1
  • Lubov Ryazanova
    • 1
  • Anton Zvonarev
    • 1
  • Ludmila Trilisenko
    • 1
  • Tatiana Kulakovskaya
    • 1
  • Mikhail Eldarov
    • 2
  1. 1.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchinoRussia
  2. 2.FRC Biotechnology, Institute of BioengineeringRussian Academy of SciencesMoscowRussia

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